Abstract
BackgroundTicks secrete a diverse mixture of secretory proteins into the host to evade its immune response and facilitate blood-feeding, making secretory proteins attractive targets for the production of recombinant anti-tick vaccines. The largely neglected tick species, Rhipicephalus zambeziensis, is an efficient vector of Theileria parva in southern Africa but its available sequence information is limited. Next generation sequencing has advanced sequence availability for ticks in recent years and has assisted the characterisation of secretory proteins. This study focused on the de novo assembly and annotation of the salivary gland transcriptome of R. zambeziensis and the temporal expression of secretory protein transcripts in female and male ticks, before the onset of feeding and during early and late feeding.ResultsThe sialotranscriptome of R. zambeziensis yielded 23,631 transcripts from which 13,584 non-redundant proteins were predicted. Eighty-six percent of these contained a predicted start and stop codon and were estimated to be putatively full-length proteins. A fifth (2569) of the predicted proteins were annotated as putative secretory proteins and explained 52% of the expression in the transcriptome. Expression analyses revealed that 2832 transcripts were differentially expressed among feeding time points and 1209 between the tick sexes. The expression analyses further indicated that 57% of the annotated secretory protein transcripts were differentially expressed. Dynamic expression profiles of secretory protein transcripts were observed during feeding of female ticks. Whereby a number of transcripts were upregulated during early feeding, presumably for feeding site establishment and then during late feeding, 52% of these were downregulated, indicating that transcripts were required at specific feeding stages. This suggested that secretory proteins are under stringent transcriptional regulation that fine-tunes their expression in salivary glands during feeding. No open reading frames were predicted for 7947 transcripts. This class represented 17% of the differentially expressed transcripts, suggesting a potential transcriptional regulatory function of long non-coding RNA in tick blood-feeding.ConclusionsThe assembled sialotranscriptome greatly expands the sequence availability of R. zambeziensis, assists in our understanding of the transcription of secretory proteins during blood-feeding and will be a valuable resource for future vaccine candidate selection.
Highlights
Ticks secrete a diverse mixture of secretory proteins into the host to evade its immune response and facilitate blood-feeding, making secretory proteins attractive targets for the production of recombinant anti-tick vaccines
De novo assembly and validation of the R. zambeziensis transcriptome To assemble the salivary gland transcriptome of R. zambeziensis, between 22 and 37 million paired HiScanSQ sequencing reads were generated for each time point, together with about 22 million paired MiSeq reads from a pool of all time points (Additional file 1: Table S1)
An abundance of secretory protein transcription was seen in the salivary glands, the organs in close proximity to the host that are actively expressing proteins to orchestrate host immune modulation
Summary
Ticks secrete a diverse mixture of secretory proteins into the host to evade its immune response and facilitate blood-feeding, making secretory proteins attractive targets for the production of recombinant anti-tick vaccines. Chemical acaricides have always been the most effective mechanism of tick control [4], but the emergence of acaricide-resistance [5] and health concerns due to chemically residues in meat, milk and the environment [6] have shifted the focus of tick biologists to the development of recombinant anti-tick vaccines [7,8,9,10]. Since a large number of recombinant tick proteins have been investigated and tested for protection efficiencies in hosts, with some showing very promising efficacy values (reviewed in [10]). Even though recombinant anti-tick vaccines have been shown to be attractive for tick control, their practical development has proven difficult as only two anti-tick vaccines have been commercialised to date, both targeting the same R. microplus Bm86 gut protein [12, 13].
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